Implementation of a Mindful Walking Intervention in Breast Cancer Patients After Their Primary Oncologic Treatment: Results of a Qualitative Study Within a Randomized Controlled Trial

Background: Breast cancer survivors often suffer from diagnosis- and therapy-related long-term side effects, such as cancer related fatigue, restricted stress resilience and quality of life. Walking as a physical activity and mindfulness practice have been shown to be helpful in studies. The aim of this study was to compare the individual experiences and subjectively perceived effects of walking in combination with mindfulness practice with moderate walking alone in breast cancer patients. This paper focuses on the qualitative results of a mixed-methods pilot study. Methods: Breast cancer patients who had finished their primary oncologic treatment at least 6 months ago were randomized to an 8-week group intervention program of either mindful walking or moderate walking. Within the qualitative study part, semi-structured focus group interviews (2 interviews per study arm) were conducted and analyzed using a qualitative content analysis approach. Audio recorded interviews were transcribed verbatim and pseudonymized. The subsequent data analysis was performed by using MAXQDA®. Results: A total of 51 women (mean age 55.8 [SD 10.9] years) were included in the RCT, among these 20 (mean age 56.7 [SD 12.0] years) participated in the focus group interviews (n = 11 patients of the mindful walking group; n = 9 patients of the walking group). Breast cancer patients in both groups described different effects in the complex areas of self-efficacy, coping, body awareness and self-reflection. While mindful walking primarily promoted body awareness and inner strength by mindfulness in breast cancer patients, moderate walking promoted self-efficacy by a confidence of their body and an easily integrated and accepted way of physical activity. Conclusions: Study interventions and the study setting triggered processes and reflections on one’s own health and situation. However, mindful walking and moderate walking seem to address different resources. This important knowledge may help oncologists and other therapists to assess what type of interventions can best meet the needs and requirements of individual patients. Trial registration: DKRS00011521; prospectively registered 21.12.2016; https://drks.de/search/de/trial/DRKS00011521

this context about 50% of all cancer patients, especially BC patients, use integrative medicine within the course of theirdisease 4,5 .Integrative oncology has been defined as "patient-centered, evidence-informed field of cancer care that utilizes mind and body practices, natural products, and/ or lifestyle modifications from different traditions alongside conventional cancer treatments.Integrative oncology aims to optimize health, quality of life, and clinical outcomes across the cancer care continuum and to empower people to prevent cancer and become active participants before, during, and beyond cancer treatment." 6Physical activity and mindfulness-based interventions may be considered as part of a mind-body oriented lifestyle intervention in the frame of integrative oncology.[9][10] In order to explore possible combined effects of these interventions we developed a new study intervention comprising walking elements and mindfulness meditation (mindful walking [MFW]).
The aim of this study was to compare the individual experiences and subjectively perceived effects of MFW with moderate walking (MW) alone in breast cancer patients. 11Identifying differences in the mode of action of the 2 study groups could be of interest for clinical practice regarding recommendations for patients and further research.This article focuses solely on the qualitative results of the trial and describes them in detail.

Study Design and Ethics Approval
The qualitative study part was nested in a randomized controlled, 2-armed, mixed-methods pilot study, carried out at the Institute for Social Medicine, Epidemiology and Health Economics, Charité-Universitätsmedizin Berlin, Germany from 2016to 2018.The mixed-method results of the study were published elsewhere with a focus on the quantitative part. 11ualitative research aims to describe, openly explore, and understand "from within," meaning to include subjectivity, individuality, the situation, reflections and interactions. 12The qualitative study component was chosen to explore subjective and individual experiences and perceptions in more depth and to gain a more comprehensive understanding of the similarities and differences between the 2 intervention groups.
The study was approved by the ethics committee of the Charité-Universitätsmedizin Berlin (EA1/201/16; 06.07.2016) based on the Declaration of Helsinki and ICH E6 Guideline for Good Clinical Practice (GCP).Written informed consent was obtained from all individual participants included in the study.This article follows the Standards for Reporting Qualitative Research (SRQR) (Supplement 1). 13

Participants
Inclusion criteria were female BC patients, ≥18 years of age, who had completed their primary cancer therapy (operation, chemotherapy, radiation therapy) at least 6 months before the beginning of the study intervention.Further inclusion and exclusion criteria are presented in detail in the mixed-method paper. 11For the qualitative study component all participants who had attended at least 6 out of 8 course dates, were contacted after the follow-up time of 16 weeks or longer and invited to participate in the focus group interviews.We assumed that a minimum number of 6 attended course dates was relevant to evaluate the intervention appropriately.Participation in the focus groups was voluntary.

Study Interventions
After randomization, participants of both groups, MFW and MW, attended a 90-minute group intervention once a week for 8 weeks.A maximum number of 10 participants per group was determined in advance as the maximum group size on the recommendation of the qualified and experienced trainers, as their experience has shown that courses of this type are then more feasible.
Participants of MFW performed mindfulness meditation exercises such as breathing meditation, Metta meditation (loving kindness) and body scan in combination with short walking sessions.Participants of MW only practiced moderate walking outside without mindfulness meditation exercises.Both groups were encouraged by their trainers to perform the respective intervention as a home practice.Further details are given elsewhere. 11

Qualitative Data Collection and Analysis
The qualitative data collection took place after the quantitative evaluation at a follow-up time of 16 weeks.A longer time period between the end of the follow-up time and the focus group interview came about, to bring together course participants from different MFW or MW courses in the interviews.
Two focus groups per study arm were planned in advance and conducted by M.S. and B.S., 2 experienced qualitative researchers and part of the research team.Focus groups were conducted because they represent a shared space of experience.Thus, according to Mangold "collective interactions" of the respective group intervention can be pointed out. 14rior to qualitative data collection the research team developed an interview guideline including the following topics (Figure 1-Interview Guideline): -subjectively perceived experience of course participation -significance of course participation in the frame of the BC disease -subjectively perceived effects of course participation on everyday life -feasibility of course participation The focus group interviews were recorded digitally, transcribed verbatim and pseudonymized.The following data analysis was carried out deductively and inductively using a qualitative content analysis approach. 15Codes were created both deductively based on the interview guideline and inductively from text data material.Subsequently, the codes were discussed by the qualitative researchers and the research team and decided upon in a consent procedure.Furthermore, based on Grounded Theory, memo writing was used as an analytic element.Memos are notes that function as a description to help to describe, further develop, and reflect the codes throughout data analysis. 16The data analysis was performed using the computer program MAXQDA ® .
Data analysis and its results were discussed regularly in addition in an interdisciplinary qualitative working group

Questions 1. Opening
I am very pleased that you have agreed to participate in the focus group interview as part of this study.-What was it that you were missing?

Motives and obstacles to study participation
If you look back: -What was your motivation for participating in the study?-What were the possible obstacles for study participation?

Closing
Would you like to add anything else that is important to you and has not been addressed?Thank you very much for participating in the focus group interview.
(Qualitative Research Network, Charité-Universitätsmedizin Berlin) to consider different perspectives and to ensure intersubjectivity and trustworthiness.Thus, the quality and validity of the qualitative data analysis was improved.The research team consisted of 4 physicians: 3 specialized in integrative medicine, 2 experienced in qualitative research, and 1 with a specialization in anthropology.

Results
The study was conducted between September 2017 und April 2019.Fifty-one patients were included in the mixedmethod study and randomized into groups (MFW n = 24; MW n = 27); 32 patients were contacted to take part in the focus group interviews after the follow-up period.On a voluntary basis, 20 patients agreed to participate in 4 focus group interviews, 2 focus group interviews per study arm; 12 patients declined participation in the focus group interviews mainly due to time constraints and management.The focus group interviews consisted of 4 to 6 participants each.All interviews took place at the Institute for Social Medicine, Epidemiology and Health Economics, Charité-Universitätsmedizin Berlin.The mean age of focus group participants was 56.7 years (SD 12.0).The following codes emerged deductively and inductively from the focus group interviews: evaluations and effects of course participation, doubts and criticism, reference to nature, suggestions for improvement, questionnaires, diaries, refresher course, study participation, the group, conventional medicine vs. integrative oncology, support groups, ambivalence and interaction and group atmosphere.The main codes partly contained further subcodes in a second, third and fourth level.
The following 6 central categories emerged from the relationships and interactions of the codes (Figure 2): experience of the group, changes in body experience, integration of the interventions in social life, the concept of self-efficacy, ambivalence in dealing with the BC disease and the demand for integrative oncology.In the following, these categories are to be explained in detail and compared between groups.*This code refers to conspicuousness within the focus group interviews such as parts of speech, mood, intonation of what was said, atmosphere and non-verbal behavior.In addition, interaction between the participants are included under this code, for example, reference to each other, initiation and deepening of a topic in the interaction between the participants, weighting of a topic by interview participants.The codes are supplemented and completed by explanatory memos.

Experience of the Group
The following aspects emerged regarding the group experience in both MFW and MW: Participants of both groups emphasized the importance of a group of women affected by BC, who could build on the commonality of the disease: "It is a protected space, but on the other hand it is also open for those who are inside, and you don't have to explain yourself."MFW_8, MindfulWalking_II However, there was a strong demarcation from existing support groups (see also Ambivalence in Dealing with the BC Disease).In distinction to support groups, participants of both groups emphasized the importance of the common task respectively walking and/or meditation within the framework of the group intervention.
The possibility of the exchange of experiences among BC patients along the course was positively emphasized by participants of MW.

Changes in Body Experience
Throughout the study, participants of both groups described a change in their body experience, however MFW and MW differed in their effects.MFW participants described that they became more aware of their bodies.Participants of MFW learned to deal with their bodies, which may have changed externally and internally as part of their BC treatment, and to accept their bodies and their new physicality.

"I just got a different body awareness [. . .]." MFW_9, MindfulWalking_II
In contrast, participants of MW emphasized that active walking enabled them to experience their bodies positively again.The participants reported a feeling of "positive exhaustion" through physical activity, whereas the primary cancer treatment was often characterized by negative exhaustion.

Integration of the Interventions Into Social Life
Regarding the integration, feasibility, and acceptance of the interventions in the social environment and life, there were clear differences between MFW and MW.
MFW offered an opportunity to integrate a moment of "respite" in everyday life, to focus on and increase awareness of oneself, one's surroundings and needs.However, at the same time, it was seen as difficult to integrate mindfulness into the everyday life and one's (work) environment: the concept of mindfulness might be unrealistic in an achievement-oriented society and actions of self-care may provoke reactions of astonishment and incomprehension in the social environment.It was discussed that the expansion of personal space through the formulation of one's own needs or limitations may allow new boundaries to emerge within a society, a group, or a family at the same time.Nevertheless, especially the increase of self-care was positively experienced by the participants.MW, on the contrary, was reported to be easily integrated into the daily routine and seen as a socially accepted opportunity to do something good for oneself.

"Since the beginning of March [. . .], I have been able to integrate [this] at my work [. . .] and now I go myself twice a week during working hours [. . .]. We do half an hour twice a week and it goes down well and I feel totally comfortable doing it [. . .]." MW_9, Walking_II
However, it became apparent that after completion of the primary cancer treatment for both MW and MFW, even a fixed appointment once a week can be more difficult to integrate in one's daily life due to the increased multiple burdens of work commitments, household, and family.

Experience of Self-Efficacy
A central category and effect of both interventions was the promotion of self-efficacy, however generated in 2 different ways through MFW and MW.
MFW participants emphasized an "inner strength," which was developed, trained, and promoted through mindfulness meditation as well as the strengthening of a conscious and self-determined way of dealing with oneself, one's possibilities and limits.With the help of the MFW intervention, participants learned to take themselves more seriously and to focus on themselves and their own needs.This way of self-care led to an increase in self-efficacy.In contrast, MW participants described an increase in confidence of their physical performance through MW (see Changes in Body Experience).Self-efficacy is strengthened through MW itself, because it offers a means to care for oneself, as well as the positiveness of doing something good for oneself and one's health.

"Yes, [. . .] I don't know, there is [. . .] this concept [of] selfefficacy [. . .] and [walking] is such a method, with which you can very quickly [. . .] do something good for yourself and [. . .] pat yourself on the back and say, 'you've done well now' [. . .]." MW_7, Walking_II
The positive experience of nature was taken up by both intervention groups.MFW participants emphasized the increased attention and perception of nature as something beautiful.The conscious perception of nature in everyday life was seen as a way to be mindful.MW participants, however, felt that moving in nature was directly relaxing.Movement in nature allowed them to take time out from everyday life.

Ambivalence in Dealing With the BC Disease
The statements made by participants of both groups, MFW and MW, revealed a certain ambivalence in dealing with their BC disease.Participants described a need to pick up the topic of their BC disease and its consequences again and to continue dealing with it.Nonetheless, participants also depicted a desire to leave the BC disease behind and to allow oneself to be healthy again.This inner conflict and ambivalence were reflected in various points: recognition and criticism of the questionnaires; the emphasis on the importance of having a group of affected BC patients versus the strong criticism of BC support groups; as well as motives and possible obstacles to study participation.

Demand for Integrative Oncology
Participants of both groups confirmed the importance of complementary medical treatment offers for BC patients during and/or after primary cancer therapy.Using complementary medicine, patients would regain a sense of control and self-efficacy, which they had often given up on and missed in the context of primary cancer therapy.Whereas in the standardized post-primary oncologic care setting, individual wishes and needs often remained disregarded, they were perceived and considered during both interventions.A desire for a more bio-psycho-social treatment approach especially in the aftercare of BC patients was evident in both groups.As a result, there was a demand for more integrative medicine offers in the context of cancer treatment and aftercare and, accordingly, an expansion of IO.

Summary
The results of the qualitative study show the influence of both study interventions on illness, experience and coping, body perception regarding awareness and physical exercise, and self-care and self-efficacy.The study interventions and the study setting obviously triggered processes and reflections on one's own health and situation although this is of course also influenced by individual aspects such as sociodemographic and clinical characteristics like the time since completion of the initial cancer treatment. 11

Strength and Limitations
This was the first study to our knowledge comparing different types of walking with a nested qualitative study that included several focus groups in the 2 different intervention groups.Both study interventions were characterized by a high relevance to everyday life: The mindful walking intervention followed an elaborate concept developed by an expert team.The concept was proofed in advance of the study regarding feasibility.Both walking interventions were easy to apply.Conducting focus group interviews provided the opportunity to elaborate collective experiences and thus come to a common consensus instead of focusing on individual experiences.
A limitation might be the sample of interviewed women: The interviewees had to have participated in at least 6 from 8 group dates, the participants who rarely came to the intervention dates or dropped out were not represented in the sample, thus a participation bias in the focus groups must be considered.In addition, the dynamic of focus groups may discourage certain participants from expressing opinions and experiences that differ from most of the other participants.Using other qualitative data collections methods, such as participatory observation of the study interventions, might have resulted in other insights. 17Another limitation might have been the varying length of the individual time between the end of the follow-up time point and the interview participation, that could have led to a recall bias.This happened because we wanted to mix participants from different courses of one intervention group.We decided for this model to avoid established group dynamics, but this also removed the familiar framework of an already known group, which could have led to more openness in the discussion.

Discussion
The following sections discuss the results of the main categories identified in the qualitative analysis.

The Role of the Group Setting
The group setting of the interventions created room for reflecting one's own situation as a member of a cancer patient group with special needs.A different acceptance and legitimation for the formulation of one's own health care needs may easily arise a group of similarly affected persons in contrast to other social contexts.The reflections in the study groups during the practice of the different interventions may have enabled an increased exchange between the patients but it was not forced.By creating a safe and "protected" space for sharing, the group setting could have contributed to the deepening and strengthening of healing therapy effects through the general effective factors described by Spiegel et al, such as shared universal suffering, mutual instilling of hope and the exchange of information, and can thus also lead to improved acceptance and coping. 18

Body Experience During Interventions
Altered body image was inductively addressed by participants in both groups during focus group interviews: MFW promoted acceptance and a conscious approach to oneself and one's own body, whereas MW activated participants and walking as such was perceived as a positive body experience.While the walking was immediately physically noticeable as outdoor exercise with subsequent perceived physical fatigue, the mindful walking rather triggered an intensified reflection process on the mental and spiritual level.The positive experiences go in line with the results of a systematic review, where Paterson et al highlight the importance of body image disturbances for young BC survivors and emphasize the need for further randomized intervention trials to assess and treat body image disturbances in BC survivors. 19Also, a further meta-analyses of 56 trials with 4826 patients have shown possible positive effects of physical activity among other on body image in cancer survivors. 8

Integration of Interventions in Social Life
Qualitative statements about the multiple burdens of professional work, household, and family of participants in both groups, as well as the time commitment as the main reason for nonparticipation in the study, dropouts, and noncompliance during the study, highlight barriers and difficulties of the interventions and are consistent with statements in the literature. 20Other studies show that the implementation of regular activities such as physical activity despite knowing about the benefits can be limited for BC patients by various, also gender-specific individual (eg, feeling guilty for taking care of yourself) or socio-cultural demands. 21,22ultiple stresses due to professional work and care work particularly affects women, highlighting existing gender inequalities in studies of female BC patients. 23Whereas MW was easy to integrate into everyday life and was socially accepted, MFW participants sometimes also reported resistance in the social environment and difficulties in applying individual mindfulness meditations.
Difficulties with individual mindfulness exercises and the large time commitment required to practice at home were also evident in a mixed-methods study by Eyles et al, who tested the feasibility of an MBSR intervention in patients with metastasized BC. 20

Self-efficacy
The disease itself, self-reflection, and training of self-care skills by interventions such as in our study leads often to a different level of self-care capabilities and self-efficacy. 24elf-efficacy, coined by Albert Bandura, can be defined as a person's belief to successfully master challenges on their own and influence events that affect one's life even in difficult situations. 25 The strong desire for self-help and active participation as a motivation for study participation as well as the development of self-care and self-efficacy through the study interventions emerged as a central aspect in the focus group interviews of both groups.These findings are comparable to results on the use of integrative medicine found in the literature.A cross-sectional study by Theuser et al showed that the need to become active oneself can be fulfilled and coping strategies improved through the use of CIM. 26 Hack et al showed that BC patients benefit from active participation and improved self-care through CIM. 27A meta-analysis by Merluzzi et al emphasized the relevance of self-efficacy as a positive resource for BC patients and as a target parameter for future studies. 28

Coping and Ambivalence
Health resources mentioned by our participants like feeling physically active (MW) and feeling connected to others and to their own fate (MFW) may not only lead to a short-term increase in well-being and the feeling of creating a room for self-care as a basis for self-efficacy, but also to a long-term improved coping with the underlying disease. 29Coping in the sense of Lazarus and Folkman helps to manage threatening situations by activating adequate resources, appraise the situation and adapt to it.Effective coping strategies include an optimistic approach, a self-confident approach and seeking social support.Ineffective coping methods include hopelessness and submissive approaches.Better coping using psychosocial interventions may influence long term survival in BC patients. 30A study of Stöckigt et al identified keeping a positive attitude toward life, choosing social contacts, and staying active as much as possible as crucial coping strategies in BC patients and found it related to quality of life. 29Further, in our study, nature as a space in which an intervention (MW) takes place and as a reference for a targeted perception training in the context of mindfulness exercises (MFW) was seen by our patients as a timeout in nature from everyday life and source for well-being, relaxation and enjoyment.That these aspects contribute to coping with cancer seems plausible.Various systematic reviews in which interventions also study different naturebased therapies support this assumption.][33] However, to deal with a chronic and possibly life-threatening disease often includes defense in the form of ambivalence in facing the illness. 34Especially "cancer-free" declared cancer survivors, like those in our study, often wish to leave the disease behind and focus unconditionally on their hard-won health.According to Kübler Ross' model of coping in severe illness, defense against the diagnosis may be an important phase that can end with acceptance of the illness, which can open up new scope for action. 35indfulness training programs with reflecting tasks can be emotionally very confrontational and thus enhance ambivalence for patients. 36,37Bisseling et al found that the right time to participate in a mindfulness-based stress reduction program for BC patients depends more on their emotional readiness to let themselves feel vulnerable than on the stage of treatment. 38This point should be considered in counseling patients.

Demand for Integrative Oncology
Especially for cancer patients, who often experienced feelings of powerlessness and loss of control due to the disease and its medical treatments, the feeling of self-efficacy and having influence on their own health remains limited sometimes. 39In this respect, health promotion interventions like in our study may empower patients by activating already known resources, such as walking, or opening up possible new resources, such as meditation.In this way, health-promoting courses from the field of physical activity and mindfulness often function as a kind of vehicle for self-efficacy in fighting or dealing with one's own disease.Cancer patients acknowledge this and demand these interventions as well as others from the field of integrative oncology. 40everal guidelines for patients with BC or other cancer highlight the role of physical activity and mindfulness interventions. 41,42In Germany, however, courses in the field of movement therapy and mindfulness, such as MBSR courses, are often only subsidized as prevention courses for healthy individuals by the statutory health insurance. 43In the context of adequate patient care, this point should be changed, especially for chronically ill patients.

Conclusion
Qualitative results of this exploratory study showed that breast cancer patients in both groups described effects of the study interventions regarding the complex areas of selfefficacy, coping, body awareness and self-reflection.In addition, the group setting of the study interventions seems to play a positive role as a framework to promote these aspects.Our main finding was that mindful walking and moderate walking seem to address different resources.While participants of MFW emphasized body awareness and inner strength by mindfulness, patients from MW experienced self-efficacy by a confidence of their body and an easily integrated and accepted way of physical activity.These insights may help oncologists and other therapists to assess what kind of interventions may meet individual patients´ needs and demands.As a result of the predominantly positive and inspiring experiences of the study patients we think that there is a high demand for more mindbody oriented offers from the field of integrative oncology in cancer patients.

3. Importance in the course of the breast cancer disease
How did you find the course and what did it bring to you personally?

. Walking course only: Relation to nature
"I deliberately said, 'No, I won't do it, I'm reaching my limit here, I can't do it anymore.[. ..]Someone else must do it.'[. ..]I didn't know that about myself [. ..], and [. ..]I noticed [. ..] that the environment had a lot of problems with it."MFW_8, MindfulWalking_II